Abstract
Disease is increasingly recognized as a threat to coral reef ecosystems, particularly in the light of increasing anthropogenic disturbances that disrupt important symbiotic partnerships within the coral holobiont. White syndromes (WSs) are a prevalent group of coral diseases in the Indo-Pacific region that have been the focus of an increasing number of investigations over the past decade. Here, we summarize the current state of knowledge on WSs, advocate the use of established standardized criteria to describe disease lesions at gross and cellular levels to move the field forward, and highlight potential erroneous characterization of underlying causes that hinders ongoing progress in coral disease research. We argue for retention of the general term WSs for Indo-Pacific cases of tissue loss lacking distinguishing macroscopic signs and with unknown aetiologies, but erection of more specific names once standardized criteria are met. Recent advances in WS disease pathology, microbial ecology, physiology, ecology and environmental drivers are discussed and the need for greater application of interdisciplinary approaches is emphasized. Following recent widespread reports of WSs on coral reefs, a clear, concise perspective is needed to provide a focus for further research and avoid confusion in the study of this virulent group of diseases.
References
Aeby G (2005) Outbreak of coral disease in the Northwestern Hawaiian Islands. Coral Reefs 24:481
Aeby GS, Work T, Fenner D, di Donato E (2008) Coral and crustose coralline algae disease on the reefs of American Samoa. In: Proc 11th Int Coral Reef Symp, pp 197–201
Aeby GS, Bourne DG, Wilson B, Work TM (2011) Coral diversity and the severity of disease outbreaks: a cross-regional comparison of Acropora white syndrome in a species-rich region (American Samoa) with a species poor region (Northwestern Hawaiian Islands). J Mar Biol 2011:1–8
Aeby GS, Ross M, Williams GJ, Lewis TD, Work TM (2010) Disease dynamics of Monitpora white syndrome within Kaneohe Bay, Oahu, Hawaii: distribution, seasonality, virulence, and transmissibility. Dis Aquat Org 91:1–8
Ainsworth TD, Hoegh-Guldberg O (2009) Bacterial communities closely associated with coral tissues vary under experimental and natural reef conditions and thermal stress. Aquat Biol 4:289–296
Ainsworth TD, Vega Thurber R, Gates RD (2010) The future of coral reefs: a microbial perspective. Trends Ecol Evol 25:233–240
Ainsworth TD, Kvennefors EC, Blackall LL, Fine M, Hoegh-Guldberg O (2007a) Disease and cell death in white syndrome of Acroporid corals on the Great Barrier Reef. Mar Biol 151:19–29
Ainsworth TD, Kramasky-Winter E, Loya Y, Hoegh-Guldberg O, Fine M (2007b) Coral disease diagnostics: What’s between a plague and a band? Appl Environ Microbiol 73:981–992
Anthony SL, Page CA, Bourne DG, Willis BL (2008) Newly characterized distinct phases of the coral disease ‘atramentous necrosis’ on the Great Barrier Reef. Dis Aquat Org 81:255–259
Antonius A (1985) Coral diseases in the Indo-Pacific: a first record. PSZNI Mar Ecol 6:197–218
Ban SS, Graham NAJ, Connolly SR (2012) Relationships between temperature, bleaching and white syndrome on the Great Barrier Reef. Coral Reefs 32:1–12
Barash Y, Sulam R, Loya Y, Rosenberg E (2005) Bacterial strain BA-3 and a filterable factor cause a white plague-like disease in corals from the Eilat coral reef. Aquat Microb Ecol 40:183–189
Beeden R, Willis BL, Raymundo LJ, Page CA, Weil E (2008) Underwater cards for assessing coral health on Indo-Pacific reefs. Coral reef targeted research and capacity building for management program: Currie Communications, Melbourne, p 22
Bourne DG (2005) Microbiological assessment of a disease outbreak on corals from Magnetic Island (Great Barrier Reef, Australia). Coral Reefs 24:304–312
Bourne DG, Garren M, Work TM, Rosenberg E, Smith G, Harvell CD (2009) Microbial disease and the coral holobiont. Trends Microbiol 17:554–562
Bower SM, McGladdery SE, Price IM (1994) Synopsis of infectious diseases and parasites of commercially exploited shellfish. Annu Rev Fish Dis 4:1–199
Bruno JF, Petes LE, Harvell CD, Hettinger A (2003) Nutrient enrichment can increase the severity of coral diseases. Ecol Lett 6:1056–1061
Bruno JF, Selig ER, Casey KS, Page CA, Willis BL, Harvell CD, Sweatman H, Melendy AM (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biol 5:1220–1227
Bythell JC, Pantos O, Richardson L (2004) White plague, white band, and other “white” diseases. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Heildelberg, pp 351–364
Bythell JC, Barer MR, Cooney RP, Guest JR, O’Donnell AG, Pantos O, Le Tissier MDA (2002) Histopathological methods for the investigation of microbial communities associated with disease lesions in reef corals. Lett Appl Microbiol 34:359–364
Cho I, Blaser MJ (2012) The human microbiome: at the interface of health and disease. Nat Rev Genet 13:260–270
Dalton SJ, Smith SDA (2006) Coral disease dynamics at a subtropical location, Solitary Islands Marine Park, eastern Australia. Coral Reefs 25:37–45
Dalton SJ, Smith SDA, Harrison M, Caroll AG, Pereg L, Cairns SC (2010) Spatial and temporal patterns of Australian White Syndrome at eastern Australian reefs: host range, prevalence, and progression of tissue necrosis. In: Holmgren A, Borg G (eds) Handbook of disease outbreaks: prevention, detection and control. Nova Science Publishers, New York, pp 187–210
Denner EBM, Smith GW, Busse H-J, Schumann P, Narzt T, Polson SW, Lubitz W, Richardson L (2003) Aurantimonas coralicida gen, nov., sp. nov., the causative agent of White Plague type II on Caribbean scleractinian corals. Int J Syst Evol Microbiol 53:1115–1122
Downs CA, Kramarsky-Winter E, Woodley CM, Downs A, Winters G, Loya Y, Ostrander GK (2009) Cellular pathology and histopathology of hypo-salinity exposure on the coral Stylophora pistillata. Sci Total Environ 407:4838–4851
Haapkyla J, Seymour AS, Trebilco J, Smith D (2007) Coral disease prevalence and coral health in the Wakatobi National Park, south-east Sulawesi, Indonesia. J Mar Biol Assoc UK 87:403–414
Heron SF, Willis BL, Skirving WJ, Eakin CM, Page CA, Miller IR (2010) Summer hot snaps and winter conditions: modelling white syndrome outbreaks on Great Barrier Reef corals. PLoS One 5:e12210
Hobbs J-P, Frisch AJ (2010) Coral disease in the Indian Ocean: taxonomic susceptibility, spatial distribution and the role of host density on the prevalence of white syndrome. Dis Aquat Org 89:1–8
Jacobson DM, Smith LW, Dailer ML, Smith JE, Herzfeld I, Smith CM, Sansone F, Whelan KR, Miller J, Warra R (2006) Fine scale temporal and spatial dynamics of a Marshall Islands coral disease outbreak: evidence for temperature forcing. EOS Trans Am Geophys Union 87(36): Suppl
Jones RJ, Bowyer J, Hoegh-Guldberg O, Blackall LL (2004) Dynamics of a temperature-related coral disease outbreak. Mar Ecol-Prog Ser 281:63–77
Kawamoto T (2003) Use of a new adhesive film for the preparation of multi-purpose fresh-frozen sections from hard tissues, whole-animals, insects and plants. Arch Histol Cytol 66:123–143
Lawrence SA, Davy JE, Aeby GS, Wilson WH, Davy SK (2014) Quantification of virus-like particles suggests viral infection in corals affected by Porites tissue loss. Coral Reefs 33:687–691
Lesser MP, Bythell JC, Gates RD, Johnstone RW, Hoegh-Guldberg O (2007) Are infectious diseases really killing corals? Alternative interpretations of the experimental and ecological data. J Exp Mar Biol Ecol 346:36–44
Lightner DV (1996) A handbook of shrimp pathology and diagnostic procedures for disease of cultured penaeid shrimp. World Aquaculture Society, Baton Rouge, LA, p 304
Lightner DV, Redman RM (1998) Shrimp diseases and current diagnostic methods. Aquaculture 164:201–220
Lindrop AMM, Hind EJ, Bythell JC (2008) The unknowns in coral disease identification: an experiment to assess consensus of opinion amongst experts. In: Proc 11th Int Coral Reef Symp, pp 190–196
Luna GM, Biavasco F, Danovaro R (2007) Bacteria associated with the rapid tissue necrosis of stony corals. Environ Microbiol 9:1851–1857
Luna GM, Bongiorni L, Gili C, Biavasco F, Danovaro R (2010) Vibrio harveyi as a causative agent of the white syndrome in tropical stony corals. Environ Microbiol Rep 2:120–127
Maynard JA, Anthony KRN, Harvell CD, Burgman MA, Beeden R, Sweatman H, Heron SF, Lamb JB, Willis BL (2011) Predicting outbreaks of a climate-driven coral disease in the Great Barrier Reef. Coral Reefs 30:485–495
Myers RL, Raymundo LJ (2009) Coral disease in Micronesian reefs: a link between disease prevalence and host abundance. Dis Aquat Org 87:97–104
Page CA, Baker DM, Harvell CD, Golbuu Y, Raymundo L, Neale SJ, Rosell KB, Rypien KL, Andras JP, Willis BL (2009) Influence of marine reserves on coral disease prevalence. Dis Aquat Org 87:135–150
Pollock FJ, Morris PJ, Willis BL, Bourne DG (2011) The urgent need for robust coral disease diagnostics. PLoS Pathog 7:e1002183
Pollock FJ, Katz SM, Bourne DG, Willis BL (2013) Cymo melanodactylus crabs slow progression of white syndrome coral disease. Coral Reefs 32:43–48
Pratchett MS, Pisapia C, Sheppard CRC (2013) Background mortality rates for recovering populations of Acropora cytherea in the Chagos Archipelago, central Indian Ocean. Mar Environ Res 86:29–34
Pratchett M, Graham NAJ, Sheppard CRC, Mayes B (2010) Are infestations of Cymo melanodactylus killing Acropora cytherea in the Chagos archipelago? Coral Reefs 29:941
Raymundo LJH, Harvell CD, Reynolds TL (2003) Porites ulcerative white spot disease: description, prevalence, and host range of a new coral disease affecting Indo-Pacific reefs. Dis Aquat Org 56:95–104
Raymundo LJ, Rosell KB, Reboton CT, Kaczmarsky L (2005) Coral diseases on Philippine reefs: genus Porites is a dominant host. Dis Aquat Org 64:181–191
Raymundo LJ, Work T, Bruckner A, Willis BL (2008) A decision tree for describing coral lesions in the field. In: Raymundo LJ, Couch CS, Harvell CD (eds) Coral disease handbook: guidelines for assessment, monitoring and management. Coral Reef Targeted Research and Capacity Building for Management Program, Brisbane, Australia, pp 18–32
Roder C, Arif C, Bayer T, Aranda M, Daniels D, Shibl A, Chavanich S, Voolstra CS (2014) Bacterial profiling of White Plague disease in a comparative coral species framework. ISME J 8:31–39
Rodgers CS (2010) Words matter: recommendations for clarifying coral disease nomenclature and terminology. Dis Aquat Org 91:167–175
Roff G, Kvennefors ECE, Fine M, Ortiz J, Davy JE, Hoegh-Guldberg O (2011) The ecology of ‘Acroporid White Syndrome’, a coral disease from the Southern Great Barrier Reef. PLoS One 6:e26829
Séré MG, Schleyer MH, Quod J-P, Chabanet PCR (2012) Porites white patch syndrome: an unreported coral disease on Western Indian Ocean reefs. Coral Reefs 31:739
Séré MG, Tortosa P, Chabanet P, Turquet J, Quod J-P, Schleyer MH (2013) Bacterial communities associated with Porites white patch syndrome (PWPS) on three Western Indian Ocean (WIO) coral reefs. PLoS One 8(12):e83746
Sudek M, Work TM, Aeby GS, Davy SK (2012) Histological observations in the Hawaiian reef coral, Porites compressa, affected by Porites bleaching with tissue loss. J Invertebr Pathol 111:121–125
Sussman M, Willis BL, Victor S, Bourne DG (2008) Coral pathogens identified for white syndrome (WS) epizootics in the Indo-Pacific. PLoS One 3:e2393
Sweatman H, Cheal A, Coleman G, Delean S, Fitzpatrick B, Miller I, Ninio R, Osborne K, Page C, Thompson A (2001) Long-term monitoring of the Great Barrier Reef status report no 5. Australian Institute of Marine Science, Townsville, p 106
Sweet M, Bythell J (2012) Ciliate and bacterial communities associated with white syndrome and brown band disease in reef-building corals. Environ Microbiol 14:2184–2199
Thompson FL, Barash Y, Sawabe T, Sharon G, Swings J, Rosenberg E (2006) Thalassomonas loyana sp. nov., a causative agent of the white plague-like disease of corals on the Eilat coral reef. Int J Syst Evol Microbiol 56:365–368
Timothy RM, Shawn MM, Joanne ED, William HW, Esther CP, Kathy LP, Joseph M (2004) Observations of a new source of coral mortality along the Kenyan coast. Hydrobiologia 530/531:469–479
Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI (2007) The human microbiome project. Nature 449:804–810
Ushijima B, Smith A, Aeby GS, Callahan SM (2012) Vibrio owensii induces the tissue loss disease Montipora white syndrome in the Hawaiian reef coral Montipora capitata. PLoS One 7:e46717
Vargas-Angel B (2009) Coral health and disease assessment in the US Pacific remote Islands areas. Bull Mar Sci 84:211–227
Weil E, Irikawa A, Casareto B, Suzuki Y (2012) Extended geographic distribution of several Indo-Pacific coral reef diseases. Dis Aquat Org 98:163–170
Williams GJ, Aeby GS, Cowle ROM, Davy SK (2010) Predictive modelling of coral disease distribution within a reef system. PLoS One 5(2):e9264
Williams GJ, Knapp IS, Work TM, Conklin EJ (2011) Outbreak of Acropora white syndrome following a mild bleaching event at Palmyra Atoll, Northern Line ISlands, Central Pacific. Coral Reefs 30:621
Willis BL, Page CA, Dinsdale EA (2004) Corals disease on the Great Barrier Reef. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Heidelberg, pp 69–104
Wobeser GA (2010) Disease in wild animals, investigation and management, 2nd edn. Springer, Heidelberg p393
Work TM, Rameyer RA (2005) Characterizing lesions in corals from American Samoa. Coral Reefs 24:1–7
Work TM, Aeby GS (2006) Systematically describing gross lesions in corals. Dis Aquat Org 70:155–160
Work TM, Aeby GS (2011) Pathology of tissue loss (white syndrome) in Acropora sp. corals from the Central Pacific. J Invert Pathol 107:127–131
Work TM, Meteyer C (2014) To understand coral disease, look at coral cells. EcoHealth. doi:10.1007/s10393-014-0931-1
Work TM, Russell R, Aeby GS (2012) Tissue loss (white syndrome) in the coral Montipora capitata is a dynamic disease with multiple host responses and potential causes. Proc R Soc Lond Ser B 279:4334–4341
Work TM, Richardson LL, Reynolds TL, Willis BL (2008) Biomedical and veterinary science can increase our understanding of coral disease. J Exp Mar Biol Ecol 362:63–70
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Handling Editor Stuart Sandin
Rights and permissions
About this article
Cite this article
Bourne, D.G., Ainsworth, T.D., Pollock, F.J. et al. Towards a better understanding of white syndromes and their causes on Indo-Pacific coral reefs. Coral Reefs 34, 233–242 (2015). https://doi.org/10.1007/s00338-014-1239-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-014-1239-x